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March 2018 | Volume 5 | Article 451
REVIEW
published: 12 March 2018
doi: 10.3389/fvets.2018.00045
Frontiers in Veterinary Science | www.frontiersin.org
Edited by:
Laura Ann Boyle,
Teagasc, The Irish Agriculture
and Food Development
Authority, Ireland
Reviewed by:
Alan G. McElligott,
University of Roehampton,
United Kingdom
Christoph Winckler,
University of Natural Resources
and Life Sciences, Vienna, Austria
*Correspondence:
Maria Vilain Rørvang
mariav.rorvang@slu.se
Specialty section:
This article was submitted
to Animal Behavior
and Welfare,
a section of the journal
Frontiers in Veterinary Science
Received: 09November2017
Accepted: 22February2018
Published: 12March2018
Citation:
RørvangMV, NielsenBL, HerskinMS
and JensenMB (2018) Prepartum
Maternal Behavior of Domesticated
Cattle: A Comparison with Managed,
Feral, and Wild Ungulates.
Front. Vet. Sci. 5:45.
doi: 10.3389/fvets.2018.00045
Prepartum Maternal Behavior
of Domesticated Cattle:
A Comparison with Managed,
Feral, and Wild Ungulates
Maria Vilain Rørvang1*, Birte L. Nielsen2,3, Mette S. Herskin1 and Margit Bak Jensen1
1 Department of Animal Science, Aarhus University, Tjele, Denmark, 2 INRA, NeuroBiologie de l’Olfaction, Université
Paris-Saclay, Jouy-en-Josas, France, 3 INRA, Modélisation Systémique Appliquée aux Ruminants, AgroParisTech,
Université Paris-Saclay, Paris, France
The event of giving birth is an essential part of animal production. In dairy cattle produc-
tion, there are substantial economical and welfare-related challenges arising around the
time of parturition, and hence increased focus on efficient management of the calving
cow. Drawing on the research literature on prepartum maternal behavior, this review
compares cattle to other members of the ungulate clade with the aim of understanding
the biological basis of bovine prepartum behavior with main emphasis on dairy cows.
Ultimately, this knowledge may be used in future development of housing systems and
recommendations for the management of calving cows. Maternal prepartum behavior
varies among species, but the final goal of ungulate mothers is the same: ensuring a calm
parturition and optimal environment for the onset of postpartum maternal behavior by
locating an appropriate birth site, with low risk of predators, disturbances and mistaken
identity of offspring. Features of chosen birth sites vary among species and depend
largely on the environment, as ungulate females display a considerable ability to adapt to
their surroundings. However, within commercial housing conditions in dairy production,
the animals’ ability to adapt behaviorally appears to be challenged. Confinement along-
side high stocking densities leave little room to express birth-site selection behavior,
posing a high risk of agonistic social behavior, disturbances, and mismothering, as
well as exposure to olfactory cues influencing both prepartum and postpartum mater-
nal behavior. Dairy cows are thus exposed to several factors in a commercial calving
environment, which may thwart their maternal motivations and influence their behavior.
In addition, prepartum cattle may be more affected by olfactory cues than other ungulate
species (e.g., sheep) because they are attracted to birth fluids already before calving.
Hence, providing dairy cows with an environment where they can perform the maternal
behavior they are motivated for, may aid a calm and secure calving and provide opti-
mal surroundings for postpartum maternal behavior. Future research should focus on
designing motivation-based housing systems allowing freedom to express prepartum
maternal behavior and investigate in more detail the effects of the environment on the
welfare of calving cows and their offspring.
Keywords: behavioral plasticity, birth place, cattle, isolation seeking, maternal behavior, motivation, olfaction,
parturition
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INTRODUCTION
e event of giving birth is an essential part of animal produc-
tion. ere are substantial economical and welfare-related chal-
lenges arising around the time of parturition, and commercial
animal production have developed an extensive body of rec-
ommendations for housing and managing parturient females.
In beef and dairy production, successful management of the
calving cow aims to ensure a viable calf with no detrimental
eects for the cow. In addition, a smooth transition from dry
to lactating is important for dairy cows. To achieve these goals,
recommendations state that careful supervision during calving
and timely intervention is crucial. Hence, calving cows should
be kept in a way that enables the farmer to identify cows in
need of assistance. Recent guidelines suggest that cows should
calve in individual pens [e.g., by law in Denmark (1) and in
e Canadian Dairy Code of Practice (2)] partly based on the
nding that cows increase the distance to the herd before calv-
ing if they have the opportunity (3). ese guidelines appear
to be well suited to the behavior of parturient cows, but the
motivation underlying this behavior is not known. Are the cows
motivated to move away from the herd to avoid other cows, to
hide from disturbances in general, or are they attempting to
hide from specic threats? If the causal factors underlying the
prepartum behavior of parturient cows are not understood, is it
then certain that aspects of animal welfare related to behavioral
needs and highly motivated behavior are accounted for when
cows are kept in individual pens at calving? Keeping cows in
individual pens benet the farmers—and by extension health
aspects of dairy cow welfare—due to easier calving supervision
and assistance when needed, but does it also satisfy maternal
motivation of the cows?
e survival and development of mammalian young depends
largely on a strong mother–ospring relationship. e clade
Ungulata includes mainly precocial species giving birth to well-
developed ospring, capable of moving on their own shortly aer
birth (4). To protect their vigorous ospring, ungulate mothers
exhibit complex behavioral patterns starting in late pregnancy
and continuing through parturition and lactation (5). is dif-
fers substantially from the normal adult female behavior and
functions to provide the young with sucient nutrition, warmth,
protection, comfort, and opportunities for social transmission
of information [as reviewed in Ref. (6)]. In the domesticated
species, reproductive success has a huge impact on productivity,
and thus scientic focus has been mainly on successful parturi-
tion and subsequent lactation, and far less on the period leading
up to parturition. Both beef and dairy cattle production rely on
the cows’ ability to reproduce, but it is only in beef cattle produc-
tion that farmers depend on the ability of the cow to establish
a strong and long-lasting bond to her calf, providing it with
nutrition and protection until weaning (7). Dairy production
is based on the cow’s ability to produce milk aer removal of
the newborn calf (7), and thus selection for maternal behavior
in dairy cows may have been relaxed compared with beef cattle
due to the reduced need for post-calving maternal investment.
However, this does not take into account the inevitable need for
prepartum maternal behavior aiming to ensure smooth calvings
with few (or preferably no) complications. is will further
safeguard strong and healthy calves, as well as healthier and
more productive cows with low morbidity (Figure1). Indeed,
post-calving success is likely to be dependent on the pre-calving
success, which emphasizes the need for appropriate prepartum
maternal behavior.
A small body of literature has shed light on the prepartum
maternal behavior of the cow, although mainly under produc-
tion conditions [e.g., Ref. (8, 9)] and only to a lesser extent
under semi-natural conditions [e.g., Ref. (3, 10) further details
Ta bl e 1 ]. To date, there are only few studies on the prepartum
maternal behavior of feral cattle [Maremma cattle (11), Masai
cattle (12), Chillingham cattle (13), and Camargue cattle (14)]
and these were all carried out several decades ago. is may seem
surprising as no less than four articles over the last 40years have
pointed out the need for more comparative studies of ancestral
and domestic behavior in cattle (15–18). Given that the ancestor
of cattle, the Auroch, has been extinct for centuries (19) and
the number of feral cattle herds are very limited (Tab l e 1), one
potential approach to understanding the biology underlying
prepartum maternal behavior of domesticated cattle, is by com-
parison with other ungulate species. Studies of feral cattle may be
more likely in the future with the advent of conservation grazing
[e.g., Ref. (20)], giving more opportunity to observe prepartum
behavior under natural or low-managed conditions.
is review draws on literature from feral and commercial
cattle breeds and investigates similarities and dissimilarities to
other members of the ungulate clade. With the main emphasis
on dairy cows, our aim was to understand the biological basis of
prepartum behavior of feral cattle to improve the understanding
of motivations underlying and mechanisms causing the behavior
seen in domestic cattle today. In the future, this knowledge may
benet the dairy industry and lead to better-adapted housing
system designs and recommendations for better prepartum
management practice, which improves both eciency and ani-
mal welfare.
WHY ISOLATE?
Many ungulate studies have reported that a proportion of the
females are “hiding,” “isolating,” “being secluded,” or “seeking
away” from the herd or from other “threats” around the time of
parturition. e term “isolation seeking” is commonly used in
such studies, but what is termed isolation in one species may dif-
fer from what is termed isolation in other species. Irrespectively,
the term “isolation seeking” is used to indicate the purpose of the
behavior: to hide and seclude the female from disturbances (aris-
ing from various threats), thus allowing her to give birth in a calm
place, where she subsequently is able to nurse and bond with her
young. However, as isolation seeking in one ungulate species may
dier from that of other species, the comparison of dierent ways
to achieve the same goal is relevant, especially as the underlying
motivations of females of dierent species may or may not be
the same. In the following, isolation behavior is discussed in the
context of causality, whereas the hider/follower paradigm is dealt
with in Section “e Hider/Follower Paradigm,” although some
overlap is unavoidable.
FIGURE 1 | The impact of the prepartum search for and selection of an appropriate birth site. Prepartum success depends on the female’s ability to locate an
appropriate birth site to ensure and safeguard a calm parturition and optimal surroundings for postpartum maternal behavior by lowering the risk of predators,
disturbances, and mistaken identity of offspring. This, in turn, increases the chance of postpartum success.
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In sheep, Dwyer and Lawrence (50) suggested that birth-site
selection (termed “isolation seeking”) varies with increasing
degree of domestication. Wild and feral breeds of sheep such as
mouons, Soay, Dall, and bighorn are observed to move away
from the herd to rocky and secluded areas (51–55), hence they
may not distance themselves from the herd, but seek cover, or
a combination of the two. Domesticated breeds such as Merino
sheep also distance themselves from the herd, but only when
the environment oers a degree of elevation or topographical
change, otherwise the ewes give birth within the herd (56). is
may be inuenced by articial selection for more sociability in
the domestic breeds (50), but is evidently also aected by the
environment (see e Hider/Follower Paradigm).
So far, some ungulate studies have sought to explain pre-
partum isolation seeking behavior of females, and noted that
the characteristics of the birth site itself may be less important
than the ability to move away from disturbances (57). An
example of this can be seen in wild omson’s gazelles (58):
Roberts and Rubenstein showed that if a herd caught up with
a parturient female, the newborn fawns were usually killed by
jackals, presumably due to the group being too conspicuous. In
such cases, being disturbed by the herd can have fatal conse-
quences, and since disturbances during parturition were much
more common for non-isolating than for isolating females, the
hiding aspect of the isolation seeking behavior appears impor-
tant for the survival of the ospring in this species. Yet, other
studies indicate that fallow deer dams adapt their maternal
behavior to the prevailing predator pressure, which even may
supersede forage availability (59). is is a sensible priority as a
predator is an acute survival threat as opposed to lack of food,
which may be tolerated in the short term. Another example
of prepartum isolation comes from breeds of domestic sheep,
which move to the edges of their enclosure to lamb, thought to
be caused by disturbances arising from human activity (50).
Likewise, indoor-housed domestic sheep will use a cubicle
at lambing when given the opportunity (60, 61). In addition,
when disturbed by human activity in the area, elk dams will
change their movement pattern, especially if disturbed during
calving season (62). Assuming that wild ungulate dams per-
ceive humans as predators, such behavioral exibility, may have
originated from sensitivity to predator pressure (58). Avoiding
predators by hiding is an adaptive behavior as it reduces the
risk of having the ospring killed and these behaviors may thus
be preserved in domestic species. Hence, isolation may be a
means to avoid disturbances in general, but more specically
avoid predators or other immediate threats. Irrespectively,
in a commercial livestock production environment, where
females are surrounded by herd mates, hiding will oen be dif-
cult, especially if human activity and other disturbances are
frequent. More work is needed to examine whether domestic
females are aiming to avoid threats, and whether disturbance
may cause articial isolation opportunities to be less attractive
TABLE 1 | Overview of observations within studies of maternal behavior in cattle with main emphasis on prepartum behavior.
Feral cattle Pasture-kept cattle Cattle housed in intensive commercial
environment (mainly indoors)
Features of the birth site
Vegetative/visual cover Differs with habitath,k Differs with habitatE
Mainly visual coverA
No clear preference19
Provides cover from disturbances Not studied Yes, from herd membersACalving when quiet in the barn1,5,21
Higher stocking density results in lower
“isolation seeking”17
Distance to herd Leave the herd but no
defined distancee,g,h,i
10–380m away from the herdd
Leave the herd but no
defined distanceG
Not studied
Prepartum behavioral changes
Separation from herd Yes a,c, e,g,h,i,j
Only some cows dob,d,f
Yes A,C,E
Only some cows doF
NoB,D,H
Yes 4,16
Only some cows do6
Yes, but depends on calving difficulty19
Restlessness Yes dYes A,C,F Yes 1,3,4,10,12,21
Varies with calving difficulty2,19
Increased walking/searching Yes dYes C,F Yes 1,7,12,13,14,19,22
Lying time Not studied UnchangedGLower on the day of calving10,15
Higher 8h before calving3
Increased transition from standing
to lying and viceversa
Yes dYes A,C,G Yes 1,2,3,8,10,12,13,14,15,19,22
Increased sniffing/exploration Not studied Not studied Yes 1,14,19,22
No2
Increased tail raising Not studied Yes C,F Yes 2,11,12,13,14
Licking own body and attention
toward abdomen
Yes dYes CYes 1,10,12,22
No11
Scraping or pawing the ground Yes dYes CYes 1,22
Less feeding behavior Yes dNot studied Yes 10,12,13,14
Reduced rumination Not studied Not studied Yes 1,3,7
A role of olfaction
Licking of own birth fluids Yes dYes A,C,F Yes 1,12,14,18,20,22
Calving at own birth fluid spot Not studied Yes A,C Yes 18,20
Mismothering Not observedjYes A,B,F
Not observedG
Yes 6,9,19
Interest and sniffing from
other cows during calving
Noj
Yes f
Only from cows close to calving
themselvesd
Yes A,B,F
NoG
Yes 6,9,15,18,19
The table includes 41 studies separated into the categories: feral (n=11), pasture-kept (n=8), and intensive commercial cattle mainly housed indoors (n=22). Aspects of and
behaviors related to three different subjects (features of the birth site, prepartum behavioral changes, and the role of olfaction) are listed. Numbers and characters in superscript
indicate the corresponding reference listed at the bottom of the table, with the number in brackets after each reference indicating the order in the reference list. ‘Not studied’
refers to the authors being unable to find any literature on this specific aspect.
References: aBaskin and Stepanov (21); bFinger etal. (22); cHall (13); dKiley-Worthington and de la Plain (23); eLent (4); fLidfors and Jensen (24); gReinhardt (25); hReinhardt etal. (12);
iSchloeth (14); jVitale etal. (11); AAitken etal. (26); BEdwards (27); CGeorge and Barger (10); DLidfors (28); ELidfors etal. (3); FOwens etal. (29); GRice etal. (30); HWood-Gush etal.
(31); 1Arthur (32); 2Barrier etal. (33); 3Borchers etal. (34); 4Dufty (35); 5Edwards (36); 6Edwards and Broom (16); 7Houwing etal. (17); 8Huzzey etal. (37); 9Illmann and Špinka (38);
10Jensen (8); 11Lange etal. (39); 12Metz and Metz (40); 13Miedema etal. (41); 14Miedema etal. (42); 15Proudfoot etal. (43); 16Proudfoot etal. (44); 17Proudfoot etal. (45); 18Rørvang
etal. (46); 19Rørvang etal. (47); 20Selman etal. (48); 21von Keyserlingk and Weary (49); 22Wehrend etal. (9).
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[as suggested by Rørvang etal. (63)]. e level of disturbances
can be high in commercial environments (i.e., from humans
and conspecics), and the use of an articial hide by the cow
may reduce her perceived ability to escape a potential threat;
hence, some articial hides may not provide an attractive
birth site.
Another adaptive aspect underlying isolation is a reduced
risk of mismothering, i.e., cows licking and nursing calves that
are not their own ospring. e immediate licking and sning
of the young by the dam are part of the typical behavioral rep-
ertoire of ungulates enabling the mother to learn the odor and
features of her young for later recognition, thereby ensuring that
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her parental investment is directed toward her own ospring
(54, 64). Several studies in domestic cattle have shown that
group housed peri-parturient cows may lick alien calves, i.e.,
calves born from other cows [e.g., Ref. (27)] and cross-fostering
(i.e., when a cow adopts an alien calf by allowing it to suckle) has
also been reported [e.g., Ref. (65)]. However, observations from
feral cattle herds indicate that cows rarely nurse or lick alien
calves [Maremma cattle (11), Masai Cattle (12)]. e feral cow
and calf may develop a stronger mother–ospring bond, which
is established through intensive contact during a sensitive period
just aer parturition [potentially just a few hours aer calving
(4, 49)]. is bond may be established quicker in an undisturbed
calving environment, which may not be available for domestic
cows in a group pen. Calving in a group pen leads to an increased
risk of mismothering and failure to obtain colostrum by the
calf, thereby challenging the transfer of immunity via colos-
trum intake (27, 38). One reason for the observed mismatches
between dairy cows and alien calves may be a weakening of the
maternal motivation in dairy breeds. Even though dairy cow
maternal behavior may have been modied by genetic change,
studies from other domesticated animals [e.g., nest building in
pigs (66, 67) and mice (68)] suggest that maternal behavior is
preserved despite domestication. Although we cannot exclude
that the occurrence of mismothering reported by studies on
dairy cattle to some extent is aected by genetic change, a more
likely inuential factor is disturbances caused by the conned
environment. Taken together, the above comparison of pre-
partum maternal behavior of female ungulates suggest that the
behavior described as isolation seeking may be an expression of
birth-site selection; functioning to safeguard a calm and secure
birth process by avoiding threats and disturbances potentially
posing a risk to the survival of the female and the newborn in
terms of predation and mismothering whilst at the same time
ensuring suckling, bonding, and protection (Figure1).
WHAT ARE THE PROPERTIES OF
AN APPROPRIATE BIRTH SITE?
Natural selection favors mothers that display behavior and habi-
tat selection to enhance neonatal survival (59, 69, 70). Hence,
in a variable environment, natural selection will favor mothers
that are able to modulate and adapt their maternal behavior
including habitat selection to the prevailing circumstances. is
ability to adapt is evident in an array of maternal behaviors. For
example, if ungulates are kept in environments with few options
to search actively for an appropriate birth site, the searching
behavior displayed by the females may be less pronounced. Due
to the scarcity of dairy cow studies on these issues, this section
will draw predominately on ndings from other ungulate spe-
cies. Fouda etal. (71) reported that zoo-kept sika deer, a species
known to hide their ospring in nature, gave birth within the
herd. e authors concluded that this behavior resulted from
the lack of suitable sites where a fawn could be hidden. Lott
and Galland (72) saw some isolation seeking in American
pasture-kept bison. ey stated that the bison gave birth away
from the herd when vegetative cover oered visual isolation
from the herd, whereas calving happened within the herd when
visual isolation was not possible. Roberts and Rubenstein (58)
found that omson’s gazelle females spent considerable time
searching for a suitable place to give birth (sometimes traveling
more than a kilometer) and mainly gave birth in tall grass
away from the herd. However, the authors observed that a herd
would occasionally catch up with the parturient female, negat-
ing the eects of cover availability by their presence. For other
ungulates, clear topographical birth-site preferences have been
found. Feral goats appear to prefer birth sites protected by an
overhead or vertical cover, e.g., trees or hedges (73). Domestic
sheep are known to predominantly give birth on slopes and in
depressions in the ground or areas close to hedges and walls
(74, 75), whereas mountain sheep are attracted to high, rocky
areas with clis (51, 76). Other species, such as red and fallow
deer (59, 77, 78), pronghorn (79), elk (80), wild mouon sheep
(52), and moose (81), favor thick vegetative cover providing
visual isolation from conspecics. For these species, further
studies are needed to ascertain if such preferences are expres-
sions of motivation to isolate in terms of distance from the herd
or to hide from the herd as well as other disturbances including
predators. Cattle do not appear to show clear preferences for
specic birth-site types, even though a few studies on dairy
cows have tried, without success, to elucidate what features are
favored (27, 47). Across studies of bovine birth-site selection, the
presence of vegetative cover may play a role (3, 11, 24, 26) for
the occurrence of isolation behavior.
DOES SEPARATION DISTANCE
FROM THE HERD MATTER?
One important aspect of birth-site selection is the physical dis-
tance the parturient female moves away from the herd. In many
ungulate species, parturient females distance themselves from
the herd [zebra (82); sable antelope (83); bison (72); elk (80);
pronghorn (79); horse (84); red deer (77, 85); impala (86); goat
(87); various wild sheep breeds (51, 53, 76, 88, 89)], although the
exact distance moved by the females has received only modest
attention. e only mention of this was by Karsch etal. (76),
who found that parturient ewes of wild breeds moved more than
2km away from the herd. Many studies included distance from
the herd as part of the denition of isolation when studying
prepartum behavior of females, but only rarely noted the actual
distance. For example, Kiley-Worthington and de la Plain (23)
observed free-ranging cattle and noted that isolation seeking
was rare even though they did not include a denition of the
term other than observing cows moving 10–380m away from
the herd. e authors also noted that the herd sometimes moved
with the pre-parturient cows, thereby reducing the distance
between them, similar to the ndings by Roberts and Rubenstein
in omson’s gazelles (58). Another study by Flörcke and
Grandin (90) found that red angus beef cows moved 25–1,250m
away from the main herd when calving and the authors further
noted that 88% moved more than 100m away. One complicating
aspect of distance between the parturient female and potential
threats or disturbances in her environment is the interaction
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between the distance and the possibility to hide. For example,
when ungulates live in at and barren environments, hiding
the ospring becomes dicult irrespective of the maintained
distance to threats/disturbances. Blank etal. (91) found that for
goitered gazelles in a habitat without vegetative cover, where the
mothers were unable to visually hide their ospring, distance
between mothers and ospring became crucial for the mother
not to attract predators to the young. As the mother was unable
to visually hide the ospring, she increased the distance to the
ospring, seemingly to compensate for the lack of vegetative
cover. is was shown in pronghorn mothers living on mixed-
grass prairies, where the mothers separated themselves on aver-
age 269m from the young (92). In other words, these mothers
distanced themselves to where the young was hiding when cover
was decient indicating that the increased distance was moti-
vated by protection of ospring from predators. Unfortunately,
no data are available for domesticated ungulates kept under
natural conditions, but the above ndings suggest that cover
is an important part of birth-site selection, and that parturient
females only relocate long distances insituations where physical
cover is limited.
Although isolation, hiding, seclusion, and seeking away
can all be part of prepartum behavior of ungulates, it may be
more appropriate to use “birth-site selection” to describe the
ultimate (functional) causation of the behavior observed. Female
ungulates appear to favor birth sites providing protection from
predators as well as conspecics, and the preferences of the dams
seem largely to depend on the environment. During the selection
of a birth site, physical cover may be an important factor, but
insituations where such cover is limited, distance from the herd
may become increasingly important.
THE HIDER/FOLLOWER PARADIGM
Within ungulate species, two dierent peri-parturient types are
described in the literature; these are the “hider” and “follower”
strategies of ungulate ospring and mothers (4, 51, 87, 93).
However, comparative research within ungulate species has
shown that the hider–follower dichotomy may be overly simplis-
tic, and that a number of species may be either, depending on
the circumstances. us, instead of being either/or, in reality,
hiding and following strategies may form part of a continuum,
and both of these are considered antipredator strategies. Hiders
provide protection in terms of hiding the young in covered or
secluded habitats aer giving birth (4), while followers actively
look out for and avoid predation in open habitats by keeping their
ospring close (4, 93). Incorporated into the continuum of these
two behavioral types is the dependence on the environment, and
at present little is known about the extent to which the behavior
of an individual ungulate mother and young varies depending on
variations in the environment.
It is suggested (87) that goats, which are considered typical
hider species, were only able to express “true hider character-
istics” when kept in their natural environment. In accordance,
Tennessen and Hudson (94) found that in domestic goats, early
mother–kid contact shared more characteristics with the behav-
ior of follower species. ese authors suggested that either the
hider characteristics of goats were lost through domestication
or maternal behavior changed when the animals were kept in a
dierent environment. Later, studies of goat behavior showed that
domestic goats do separate themselves from herd mates before
kidding (95). Also, their rather complex hider behavior appears
to be largely genetic, making it a highly motivated behavior and
thus less prone to evolutionary dilution (96), even though it may
be inuenced by environmental factors.
Feral populations of ancient cattle breeds living in large
and non-managed nature reserves may provide insight into
the maternal behavior of non-domesticated cattle. Cows from
African and Camargue cattle herds have been observed leaving
the herd days or hours before parturition (4, 12, 14, 25). Calves
of Chillingham cattle hide aer birth (97), whereas calves of
Maremma cattle exhibit both hiding and following behavior in
the early weeks of life depending on the availability of cover (11).
Similarly, studies in domestic cattle seem to support the above
suggestion of a lack of a strict hider/follower dichotomy. ere
are reports of cattle seeking away from the herd before birth when
kept in large, open, and non-managed natural environments
(4, 11–14, 21, 25), when pasture-kept (3, 10, 26) and when housed
under commercial production conditions (44), but many studies
report only some cows or no cows separating themselves from
their herd mates (Tab le 1). As with sheep, the studies listed in
Ta bl e 1 indicate that prepartum separation is more common in
feral types of cattle, whereas studies of pasture-kept or indoor-
housed cattle rarely report such behavior. is may be due to
domestication favoring less fearful, more social animals, which
are more stressed by social isolation as suggested for sheep (50)
or, perhaps more likely, due to the conned environment in
which the animals are usually kept. ere is not enough evidence
to suggest that domestic cattle display dierent intermediates of
hider and follower strategies although cattle may adapt to the
environment they inhabit.
PREPARTUM BEHAVIOR
In wild ungulate species, only few observations on female pre-
partum behavior have been recorded (as opposed to postpartum
behavior studies), which may be caused by the animals not
being present near the herd around parturition. Within studies
of ungulates kept under commercial housing conditions, most
authors describe some of the following behavioral changes
occurring as parturition approaches: pacing, pawing, circle
walking without an obvious goal, frequent postural changes,
and reduced lying duration [domestic goat (96), domestic sheep
(98–100), and red deer (85)]. In cattle, similar prepartum behav-
ioral changes have been described (Tab l e 1 ). Restlessness is the
behavior most oen reported in cows when calving is imminent
(Tabl e1 ). ere is, however, a discrepancy in the interpretation
of the described restlessness: is it caused by motivation to search
for an appropriate birth site, the experience of pain, or is it a sign
of frustration? e causation for the restless behavior prepartum
and during labor is currently not fully understood. e process of
giving birth is most likely painful (101), and pain may therefore
be involved in the behavioral changes prepartum. e behaviors
observed at this time (reduced lying, increased walking, walking
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with no obvious goal, reduced eating, pawing, pacing along
fences, and more frequent posture changes; Tab le 1) are all oen
interpreted as signs of restlessness and thus the denition of
restlessness varies considerably between studies. So, even though
these behaviors may all reect the same motivation of locating
an appropriate birth site, the constraints of the conned environ-
ment may cause the restless behavior. Similar arguments have
been put forward by Wass etal. (85), who suggested that fence
line pacing in pre-parturient red deer may be a result of the hind
being thwarted in searching for and locating an appropriate birth
site. Other authors have suggested that high stocking density or
low inter-individual distance may cause pacing or restlessness
due to the inability of the female to distance herself from the
herd (85, 98). Studies quantifying prepartum behavioral changes
in cattle with the aim of predicting calving time have failed to
identify a specic type of behavior, which reliably predicts the
timing of calving [e.g., Ref. (34, 102)]. However, it is agreed that
a combination of several behavioral indicators improves estima-
tion of calving time, as any one behavioral indicator cannot
reliably predict time of calving [e.g., lack of rumination 70% in
sensitivity and specicity (103)]. One possible explanation for
these ndings may be that all behavioral changes at this time
are aected by the same underlying motivation, or thwarted
motivation, to search for and nd an appropriate birth site. If so,
the apparent absence of reliable behavioral indicators may reect
dierent attempts to adapt to the situation, which depends on
environmental factors (8, 30, 37, 42, 104, 105).
Focusing on lying behavior, Huzzey et al. (37) measured
frequency and duration of standing in cows kept in individual
pens on the day of calving, and compared this with the behavior
of the same cows before and aer calving, when they were group
housed in free-stalls. Stocking density remained the same (one
cow per stall), but the environment changed markedly on the day
of calving, i.e., from group to individual housing. e authors
found reduced lying time corresponding to an approximately
2h reduction, and 80% more standing bouts on the day of calv-
ing. Jensen (8) and Miedema etal. (42) also found reductions
in lying time on the day of calving (1.3 and 1h, respectively), as
well as increased frequency of lying bouts in the last 6h before
calving. In these studies, the cows had more time (i.e., several
days) to adjust to the environment before calving than the cows
studied by Huzzey etal. (37) (which had 24h or less). In contrast
to these ndings from indoor calving studies, a recent study
by Rice etal. (30) found no reduction in lying time and only
an increase in lying bouts 3–4h before calving in cows calving
on large pasture. erefore, it is possible that the behavioral
responses observed as calving approaches are signs of failed
behavioral attempts to adapt to the conned environment.
If so, restlessness may be a sign of frustration resulting from the
cow not being able to search for and nd an appropriate birth
site, rather than a sign of stress or pain induced by parturition
per se. One might argue that as birth-site selection behavior
is observed in large and open environments, restlessness may
be seen in the conned environment because the calving cow
moves as if she was in the large environment. e behavior is
similar, but the environment aects its expression and hence its
interpretation.
Frustration from being prevented from performing pre-
partum maternal behavior has been documented in at least
one ungulate, the domestic pig. Crating of parturient sows, as
is typically done in commercial housing systems, prevents the
choice of nesting site [feral sows will walk kilometers to choose
an appropriate nesting site (66)] and prevents the performance
of natural prepartum nest building mainly due to lack of space
and lack of nesting materials (106, 107). e higher activity level
measured pre-farrowing, such as frequent changes between
standing and lying (108, 109), is most likely a reection of the
inability to search for a nesting site. Abnormal behaviors such
as bar biting (110–112), rooting the oor, and sham chewing
(111, 113) are also seen in the period leading up to farrowing.
Moreover, loose housed sows provided with pre-formed nests
still perform nest building behavior (114) and thus achieving
the goal of having a nest does not satisfy this behavioral need.
e high activity level and the abnormal behaviors may reect
the same underlying cause as the restlessness seen in cattle
and many sow studies suggest that these are signs or out-lets
of frustration arising from not being able to express the highly
motivated prepartum maternal behavior. is view is further
supported by the ndings that preventing sows from nest build-
ing activities results in decreased oxytocin levels (113, 115),
increased cortisol concentrations (111, 116), and increased
heart rate (117), leading several authors to propose that impair-
ment of natural behavior during the prepartum period results
in compromised welfare of sows (111, 117–119). Also, conned
sows have longer farrowing durations and longer inter-piglet
birth intervals, thereby challenging the vitality of the ospring
(107). Such measurements are not available within studies of
prepartum behavior of cattle but we do know from work on
social isolation and lying deprivation [measured as ACTH
increase in Ref. (120)] that non-parturient cows show signs of
frustration. In cows, more studies of the consequences of allow-
ing the possibility to perform prepartum maternal behavior
are needed to understand the motivational background of the
prepartum behavior observed in cows in commercial produc-
tion systems. Such studies would enable evaluation of whether
and when motivation-based systems mitigates the expression of
prepartum behavior, thereby improving the welfare of calving
cows and their calves.
A POSSIBLE ROLE FOR OLFACTION?
Olfaction is an aspect of maternal behavior in cattle which has
received little scientic attention until now. In many ungulate
species, birth uids are attractive and consumed by parturient
females, e.g., domestic and wild sheep (4, 56, 98, 121), horses,
pigs and goats (122), sable antelopes (123), and red deer (85),
but this behavior has only been studied sparsely in relation
to ungulate mothers’ selection of birth site. However, the
attractiveness of birth uids is closely related to parturition.
In sheep, the attraction has been shown to last for a few hours
aer lambing (121), whereas cows show signs of attraction as
early as 12h before calving lasting for at least 24-h postpartum
[the duration of the study (124)]. George and Barger (10) found
that parturient cows remained within the same area where
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their amniotic uids were discharged until calving had been
completed, and recently Rørvang et al. (46) suggested that
cows predominantly would calve at the spot where another
cow had previously calved. Attraction to olfactory cues there-
fore appears to have implications for the prepartum maternal
behavior of cattle. Maternally motivated cows kept in groups
are inevitably aected by the odor cues in the birth uids of
other cows even before giving birth themselves, and this may
be exacerbated when housing conditions prevent cows from
avoiding these odors. In addition, the attractiveness of these
odors may reduce the likelihood of a cow moving away to nd a
birth site elsewhere, which may make articial hides less attrac-
tive (63). Based on the above, we suggest that olfactory cues
need to be considered in future prepartum maternal behavior
studies and are likely to inuence the use of any calving facility
provided.
Olfactory cues, however, are not only important for the
prepartum behavior of female ungulates. In sheep, the role of
olfaction is essential for the onset of lamb-directed maternal
behavior, at least for inexperienced mothers (125, 126). For
instance, Basiouni and Gonyou (125) showed that fostering of
alien lambs to parturient females was possible only if the lambs
were covered by jackets soaked in amniotic uid. Adult domestic
goats show interest in alien newborn kids (95), and in farmed
red deer such attention can be rather intense and even increase if
stocking density is high [in addition, more mismothering occur
in this situation (85)]. As mentioned earlier, also cattle studies
have reported attention from cows toward and licking of alien
calves, especially in commercial housing conditions (Tabl e 1 ).
Studies from free-ranging cattle, however, oen do not report
cows showing interest in alien calves’, which may be explained by
the cows seeking away from the herd (11). Hiding or separating
from conspecics probably lowers the risk of mothers interacting
with alien ospring in general, but physical cover may not suce
to keep maternally motivated cows away if they can smell a calf.
Recently, we oered pregnant group housed cows an opportu-
nity to select an individual pen as birth site. e presence of a
newborn alien calf in the group pen reduced the likelihood of
the cows using this opportunity (63), most likely because the
newborn calf ’s coat contained birth uids. Hence, olfaction and
odors are likely to be important for the onset and direction of
maternal behavior also in cattle.
Commercial dairy cow housing conditions oen mean high
stocking densities in a relatively barren environment oering
few options of selecting a birth site away from other cows as well
as more disturbances from human activities and conspecics.
Taken together, this means that pre-parturient cows housed in
groups are in close proximity to olfactory stimuli important for
maternal behavior, i.e., birth uids from other cows and their
calves. Unlike sheep, cattle show a preference for birth uids
also before parturition, and prepartum cows have been reported
to nurse alien calves (59, 62), observations which may explain
the higher occurrence of mismothering in commercial housing
(Tabl e1). is may also introduce a higher risk of mismothering
when cows calve in group pens when compared with parturi-
ent sheep, as ewes are not attracted to birth uids until aer
parturition (121). In addition, group housing may increase the
risk of agonistic social interactions limiting the access of bovine
mothers to their own calves. Mismothering and lack of contact
between cow–calf increases the risk of colostrum and maternal
care being allocated to alien calves, leading to failure of passive
transfer of immunity from the mother to her biological ospring.
e importance of olfaction and odors thus need to be taken into
consideration in the design of housing facilities for parturient
cattle (127), especially in relation to group housing. Implications
of group housing of calving cows need to be critically addressed
as this type of management is quite common [for example, 70%
of US dairy operations (128)], and particularly if cows and calves
are to remain together post-calving. Keeping parturient cows
in groups is normally associated with early cow–calf separation
(2) and thus if early calf nursing and cow–calf bonding are to be
ensured, housing of parturient cows in individual calving pens
appears to be necessary.
CONCLUSION AND PERSPECTIVES
Drawing on research literature on prepartum maternal behavior,
this review compared cattle to other members of the ungulate
clade with the aim of understanding the biological basis of
bovine prepartum behavior with main emphasis on dairy cows.
Prepartum success depends on the female’s ability to locate an
appropriate birth site to ensure and safeguard a calm parturition
and optimal surroundings for postpartum maternal behavior
by lowering the risk of predators, disturbances, and mistaken
identity of ospring. At present, the motivations of cows underly-
ing the apparent prepartum isolation seeking behavior have not
been fully explored. In addition, traditional concepts of ungulate
maternal behavior such as the hider/follower-dichotomy appear
overly simplistic. Based on the reviewed literature, we suggest that
more scientic focus should be given to the prepartum maternal
behavior (i.e., the phase of birth-site selection) in dairy cows,
as they are exposed to several factors in a commercial calving
environment, which may thwart their maternal motivations
and inuence their behavior and welfare. One such factor is
olfactory cues, which may exert stronger eects on prepartum
cows than other ungulate species as cows are attracted to birth
uids already before parturition. Providing dairy cows with an
environment where they can perform the prepartum maternal
behavior for which they are motivated, may facilitate postpartum
maternal behavior and success. Further research focusing on
motivation-based housing of peri-parturient cows is needed to
ascertain the importance of degree of movement and distance
from the group within the constraints of dairy housing systems.
ese studies should include eects on the welfare of calving cows
and their ospring. Ultimately, this knowledge may be used in
future development of more suitable housing and management
systems for calving cows.
AUTHOR CONTRIBUTIONS
All authors contributed to the initial idea and early discussions
underlying this review. MR did the main literature search and
selection and wrote the rst dra of the manuscript, including
gure and table.
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ACKNOWLEDGMENTS
Cathy Dwyer and colleagues, SRUC, Edinburgh, Scotland, for
fruitful discussions on thoughts and theories. Cecilie Kobeck
orsen, Aarhus University, for adding to the evolutionary
aspects of this review.
FUNDING
is work was funded by the Green Development and
Demonstration Program of the Danish Ministry of Food,
Agriculture and Fisheries, Copenhagen, Denmark and the PhD
school GSST, Aarhus University, Denmark.
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Conict of Interest Statement: e authors declare that the research was con-
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construed as a potential conict of interest.
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